Bilateral NSF/BIO-BBSRC: Modelling Light Control of Development

Changes in the light environment, caused by encroaching vegetation or seasonal progression, can alter the course of development leading to a wide variety of plant architectures. This developmental "plasticity", is a defining characteristic of plants and a prerequisite for survival, allowing adaptation to an environment in flux. Adaptive responses to nearby vegetation are often crucial in the natural environment but costly in terms of yield in a field crop. Indeed, the ability to control crop architecture in dense canopy field conditions is a priority for plant breeders. Speaking to this need, the outputs from this project will generate novel targets and predictive tools that can be used to improve plant architecture in vegetation rich environments. The project aims to fill a knowledge gap: even though light constantly tunes plant development it is still unclear how this is executed at the cellular and molecular levels. A principal aim will be to establish how light signalling is coupled to development providing the first detailed understanding of how light drives plant growth plasticity.

Plants continue to grow and develop through their life cycle and so have to maintain an active stem cell pool. In the shoot, stem cells reside in the "meristem" which is located at the shoot apex. New organ (e.g. leaf) production is controlled by a suite of developmental genes that act at the shoot apex. Our earlier work and that of others showed that light controls the rate of leaf production, leaf size and morphology, suggesting light regulates meristem function. More recently we have uncovered molecular evidence that strongly reinforces this proposition. The research programme aims to delineate the molecular path from light activated signal transduction to organogenesis, providing the first account of how light directs development. To help resolve molecular connections, that may be intricate, we will employ an integrated modelling and experimental regime. This is possible as we have already developed light signalling model framework that can be extended to incorporate meristem genes. Model simulation of different pathway structures will allow us to predict new molecular connections that can be tested in the lab. This iterative process will facilitate and improve the accuracy of pathway assembly. The model will help us to determine how different light regimes alter pathway dynamics and development, providing a system level understanding of pathway behaviour. An important outcome will be the production of a developmental plasticity model with predictive capabilities: an invaluable resource for crop improvement programmes. Model development also represents an important step toward our future aim to construct a virtual plant.

Through the plant lifecycle the phytochrome photoreceptors detect alterations in the light environment and propagate adaptive changes in plant architecture, yet it is unclear how this is executed at the molecular level. Our supporting data provide compelling evidence that light controls development via the Shoot Apical Meristem (SAM). HECTATE (HEC) transcription factors have recently been shown to control cell proliferation by regulating SAM genes. Our studies demonstrate that HECs operate through a Phytochrome Interaction Factor (PIF)-based mechanism, inferring a direct molecular link between PIFs and the SAM. This study will integrate experimental and theoretical approaches to: i) elucidate the molecular events through which light controls SAM function, ii) develop a new conceptual model for light signalling, and iii) provide technological advances in plant architecture manipulation for plant breeding. The project benefits from significant modelling and data storage/sharing resources offered by partner labs. An initial aim will be to extend our new light signalling model to incorporate HEC-PIF control of cell proliferation. Site directed expression, qRT-PCR and ChIP assays will establish whether PIFs operate externally or from within the SAM. The system will be characterised from the molecular to the whole plant level using methodologies including biochemical assays, time-resolved target gene expression and growth profiles. These data will be used for model parameterisation, while functional analysis will delineate the molecular links between HEC-PIF and the SAM. In silico testing of different circuit structures will aid the mapping of pathway connections and provide a means to understand the emergent properties of the network e.g. in different light conditions. The ultimate goal of the project will be to generate a molecular and systems level understanding of how light regulates organogenesis, providing a new paradigm for light signalling.

Outputs from this project will include novel methods to control shoot morphology and the rate of development, traits strongly associated with crop yield. Uniquely the project will offer strategies to improve productivity in vegetation rich, field conditions. Our focus therefore aligns with a BBSRC's "Sustainable Intensification" priority to investigate methods that "produce more from the same or a smaller area of cultivated land". Project aims are likely to stimulate commercial interest, which will be pursued at an early stage to allow sufficient time to exploit and protect intellectual assets (see Pathways to Impact). This together with broad scope modelling workshops for the public, will maximise opportunities to deliver social and economic impact. Embedded in the BBSRC's Systems Approaches to the Biosciences" priority area, the project will stimulate conceptual thinking around systems modelling. A significant milestone will be the development of a robust modelling framework that predicts the impact of a changing light environment on plant development. Validated models will be made publically available through open-access University of Edinburgh and community databases. The modelling effort on project will comprise an important step toward the future aspiration to develop a digital organism.
This international partnership conforms to the BBSRC's overarching priority to encourage and support the movement of researchers between the UK and overseas (see Pathways to Impact). The US PDRA will train the UK RA in tissue-specific RNA extraction methods. In return, the US PDRA will receive tuition in methods to integrate data into models and in model simulation, through a planned sabbatical to Edinburgh. Our training exchange scheme will aid project cohesion, skill development, and assist the transfer of Systems Biology methodology to the US partner lab.